Insulin-like growth factor-I regulates LH release by modulation of kisspeptin and NMDA-mediated neurotransmission in young and middle-aged female rats

Endocrinology. 2014 May;155(5):1827-37. doi: 10.1210/en.2013-1682. Epub 2014 Mar 10.

Abstract

This study investigated potential mechanisms by which age and IGF-I receptor (IGF-Ir) signaling in the neuroendocrine hypothalamus affect estradiol-positive feedback effects on GnRH neuronal activation and on kisspeptin and N-methyl-D-aspartate (NMDA)-induced LH release and on the abundance of NMDA receptor subunits Nr1 and Nr2b and Kiss1r transcript and protein in the hypothalamus of young and middle-aged female rats. We infused vehicle, IGF-I, or JB-1, a selective antagonist of IGF-Ir, into the third ventricle of ovariectomized female rats primed with estradiol or vehicle and injected with vehicle, kisspeptin (3 or 30 nmol/kg), or NMDA (15 or 30 mg/kg). Regardless of dose, NMDA and kisspeptin resulted in significantly more LH release, GnRH/c-Fos colabeling, and c-Fos immunoreative cells in young than in middle-aged females. Estradiol priming significantly increased Kiss1r, Nr1, and Nr2b receptor transcript and protein abundance in young but not middle-aged female hypothalamus. JB-1 attenuated kisspeptin and NMDA-induced LH release, numbers of GnRH/c-Fos and c-Fos cells, and Kiss1r, Nr1, and Nr2b transcript and protein abundance in young females to levels observed in middle-aged females. IGF-I significantly enhanced NMDA and kisspeptin-induced LH release in middle-aged females without increasing numbers of GnRH/c-Fos or c-Fos immunoreactive cells. IGF-I infusion in middle-aged females also increased Kiss1r, Nr1, and Nr2b protein and transcript to levels that were equivalent to young estradiol-primed females. These findings indicate that age-related changes in estradiol-regulated responsiveness to excitatory input from glutamate and kisspeptin reflect reduced IGF-Ir signaling.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aging*
  • Animals
  • Female
  • Gene Expression Regulation, Developmental / drug effects
  • Hypothalamo-Hypophyseal System / growth & development
  • Hypothalamo-Hypophyseal System / metabolism
  • Hypothalamus / cytology
  • Hypothalamus / drug effects
  • Hypothalamus / growth & development
  • Hypothalamus / metabolism
  • Infusions, Intraventricular
  • Insulin-Like Growth Factor I / administration & dosage
  • Insulin-Like Growth Factor I / analogs & derivatives
  • Insulin-Like Growth Factor I / antagonists & inhibitors
  • Insulin-Like Growth Factor I / metabolism*
  • Kisspeptins / metabolism*
  • Luteinizing Hormone / metabolism*
  • N-Methylaspartate / metabolism
  • Nerve Tissue Proteins / agonists
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neuroendocrine Cells / cytology
  • Neuroendocrine Cells / drug effects
  • Neuroendocrine Cells / metabolism
  • Oligopeptides / administration & dosage
  • Oligopeptides / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, IGF Type 1 / agonists*
  • Receptor, IGF Type 1 / antagonists & inhibitors
  • Receptor, IGF Type 1 / metabolism
  • Receptors, G-Protein-Coupled / biosynthesis
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism
  • Receptors, Kisspeptin-1
  • Receptors, N-Methyl-D-Aspartate / agonists*
  • Receptors, N-Methyl-D-Aspartate / genetics
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Signal Transduction / drug effects
  • Synaptic Transmission* / drug effects

Substances

  • Kiss1 protein, rat
  • Kiss1r protein, rat
  • Kisspeptins
  • Nerve Tissue Proteins
  • Oligopeptides
  • Receptors, G-Protein-Coupled
  • Receptors, Kisspeptin-1
  • Receptors, N-Methyl-D-Aspartate
  • insulin-like growth factor-1, rat
  • H 1356
  • N-Methylaspartate
  • Insulin-Like Growth Factor I
  • Luteinizing Hormone
  • Receptor, IGF Type 1